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Developing a new apathy measurement scale

Citation for published version:Radakovic, R & Abrahams, S 2014, 'Developing a new apathy measurement scale: Dimensional apathyscale', Psychiatry Research, vol. 219, no. 3, pp. 658-663. https://doi.org/10.1016/j.psychres.2014.06.010

Digital Object Identifier (DOI):10.1016/j.psychres.2014.06.010

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Developing a new apathy measurement scale: dimensional apathy scale

Ratko Radakovic* a, b, c, d and Sharon Abrahams a, c, d

a Human Cognitive Neuroscience-Psychology, School of Philosophy, Psychology & Language Sciences, University of

Edinburgh, UK b Alzheimer Scotland Dementia Research Centre, University of Edinburgh, UK c Anne Rowling Regenerative Neurology Clinic, University of Edinburgh, UK d Euan MacDonald Centre for MND Research, University of Edinburgh, UK

Abstract

Apathy is both a symptom and syndrome prevalent in neurodegenerative disease, including

motor system disorders, that affects motivation to display goal directed functions. Levy and

Dubois (2006) suggested three apathetic subtypes, Cognitive, Emotional-affective and Auto-

activation, all with discrete neural correlates and functional impairments. The aim of this

study was to create a new apathy measure; the Dimensional Apathy Scale (DAS), which

assesses apathetic subtypes and is suitable for use in patient groups with motor dysfunction.

311 healthy participants (mean = 37.4, SD = 15.0) completed a 45-item questionnaire. Horn’s

parallel analysis of principal factors and Exploratory Factor Analysis resulted in 4 factors

(Executive, Emotional, Cognitive Initiation and Behavioural Initiation) that account for

28.9% of the total variance. Twenty four items were subsequently extracted to form 3

subscales – Executive, Emotional and Behavioural/Cognitive Initiation. The subscale items

show good internal consistency reliability. A weak to moderate relationship was found with

depression using Becks Depression Inventory II. The DAS is a well-constructed method for

assessing multidimensional apathy suitable for application to investigate this syndrome in

different disease pathologies.

Keywords: apathy subtypes; multidimensional apathy; motivation; apathy scale;

depression; motor dysfunction

                                                                                                               *  Correspondence  to:  University  of  Edinburgh,  Department  of  Psychology,  7  George  Square,  Edinburgh,  UK,  EH8  9JZ  Tel.  +441316509867  

Email  addresses:  r.radakovic@sms.ed.ac.uk,  radakovic.ratko@gmail.com  

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1. Introduction

Apathy has been defined as reduced motivation towards goal directed behaviours

(Marin, 1996). This can often be observed overtly as a loss of energy, interests and emotion

(Marin, 1991). In a healthy population, apathy is a fluctuating state that is frequently

experienced by many individuals. This is known as selective or relative apathy, where an

individual is not interested or motivated towards particular activity (Marin, 1990). It is

observable in normal populations (Brodaty et al., 2010). However, when this state reoccurs or

becomes constant it may be indicative of underlying pathology impairing motivational

functioning and is regarded as a prevalent symptom in neuropsychiatric and

neurodegenerative populations (for review see Chase, 2011).

The concept of apathy is thought to be composed of several elements pertaining to

emotion, cognition and behaviour (Marin, 1991), the evidence for which has been observed

through a review of neurological findings (Levy and Dubois, 2006; Levy, 2012). Based on

observations of patients with prefrontal cortex and basal ganglia lesions Levy and Dubois

(2006) proposed three underlying apathetic subtypes (see Table 1). While these three

subtypes have overlapping similarities to Marin’s proposed triadic cognitive-behavioural-

emotional structure, they differ in the Auto-activation subtype, which is defined by problems

with initiation of behaviours and cognition.

Table 1. Apathy subtypes (adapted from Levy and Dubois, 2006) Subtype Description

Cognitive The inability to manage goals and cognitively strategize

with a negative impact on cognitive and action planning.

Emotional-affective Diminished integration, processing and expression of

emotional behaviours and cognition resulting in a

continuous lack of extreme affect.

Auto-activation Lessened initiation of thoughts or behaviours that are

related to functionality (i.e. lack of motor responsiveness

(akinesia) and lack of discourse (alogia, Habib, 2004)).

In Cognitive apathy, or ‘Cognitive inertia’ (Levy and Dubois, 2006) the goal directed

behaviour is reduced due to impaired cognitive functions needed to implement planned

actions. This is similar to dysfunction of executive processes, which are necessary to achieve

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goals, including planning, organisation, attention monitoring. These processes are strongly

associated with dysfunction of the dorsolateral prefrontal cortex damage (Fuster, 1999; for

review see Stuss, 2011).

Apathy and depression have overlapping symptomology (van Reekum et al., 2005)

but an important distinction exists in that apathy relates to disorders of motivation where

depression is an affective disorder (Levy et al., 1998). The Emotional-affective subtype of

apathy can be distinguished from depression due to the presence of emotional neutrality,

whereas depression results in either extreme sadness or, in the case of bi-polar affective

disorder, also happiness. It has been suggested that dysfunction of the orbito-medial

prefrontal cortex was associated with this type of apathy (Levy and Dubois, 2006). The

orbito-medial prefrontal cortex regions are connected to areas, which facilitate emotional

processing of information pertaining to goal directed behaviour (Levy and Dubois, 2006).

Damage to the orbito-medial prefrontal cortex is suggested to disrupt the flow of emotional

processing which may result in reduced processing of emotional behaviour, context or

outcome. Damage to such systems could disrupt the motivation for goal directed behaviour

due to emotional desensitisation to both positive and negative stimuli. The emotional

ambivalence may influence decision making due to lack of emotional context.

Finally, the Auto-activation apathetic deficit has been observed as early as 1981 by

Laplane (in Habib, 2004) as “loss of psychic auto-activation” associated with the presence of

structural neuroimaging abnormalities in of the globi palli and is most commonly

characterised by decreased cognitive and physical initiative activity. Specifically, lesions to

the medial prefrontal cortex and basal ganglia have been found to manifest as Auto-

activation deficits akin to apathy (Levy and Dubois, 2006). Levy and Czernecki (2007)

suggested that lesions in the basal ganglia were associated with reduced goal directed

behaviour due to disconnectivity with the frontal lobes.

The concept of apathy as multidimensional has gained widespread recognition (Marin

et al. 1991; Cummings et al., 1994; Robert et al., 2002; Sockeel et al., 2006; Starkstein and

Leentjens, 2008). Furthermore diagnostic criteria for apathy in Alzheimer’s disease and other

neuropsychiatric disorders have been proposed, based on a consensus of an international task

force of experts in neuropsychiatric symptoms in neurodegenerative disease (Robert et al.,

2009). The criteria have been sub-divided into three symptom-domains representing

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behavioural apathy, cognitive apathy and emotional apathy concordant with Marin’s original

subclassification and highlighting the need for multidimensional assessment.

However, despite this view, there is a lack of objective tools to evaluate the different

subtypes (Levy, 2012) and apathy is most typically assessed as a singular concept (for review

see Clarke et al., 2011), examples of which include Marin’s Apathy Evaluation Scale (Marin

et al., 1991), Neuropsychiatric Inventory apathy subscale (Cummings et al., 1994), the

Frontal Systems Behavioural Scale – apathy subscale (Grace and Malloy, 2001) and scales

assessing negative symptoms (Andreasen, 1982; Kay et al., 1989). In patients with

schizophrenia, research using the Scale for Assessment of Negative Symptoms has shown a

substructural structure to negative symptoms (Blanchard et al., 2006). This has prompted the

development of novel and more comprehensive assessment methods for negative symptoms

in schizophrenia, examples being the Brief Negative Symptoms Scale (Kirkpatrick et al.,

2011) and the Clinical Assessment Interview for Negative Symptoms (Kring et al., 2013).

These new methods have resulted in a new 2 dimensional substructure of negative symptoms

composed of Apathy-Avolition and Diminished Expression. The former is defined by blunted

affect and alogia whereas the Diminished expression subtype is associated with anhedonia,

asociality and avolition (Foussias and Remington, 2010). However, these profile subgroups

are fairly new concepts and the scales detecting them have only recently been used in

research practice.

The only established apathy measures that recognised the presence of an apathetic

substructure through its assessment method are the Lille Apathy Rating Scale (Sockeel et al.,

2006) and Apathy Inventory (Robert et al., 2002). The latter includes only one item per

dimension and so does not provide a comprehensive assessment, while validation of the Lille

Apathy Rating Scale in Parkinson’s Disease patients, revealed a four factor structure;

intellectual curiosity, self-awareness, emotion and action initiation (Sockeel et al., 2006)

which did not map onto the established triadic structure – of cognitive, emotional and

behavioural classifications. Further use of the Lille Apathy Rating Scale subsequently

focused on the total summative score of apathy despite evidence of multiple dimensions.

Furthermore, the limited utility of some measurements in the comprehensive assessment of

apathy is further confounded in patients with physical disability. Apathy is a common

symptom in neurodegenerative disease in which motor system dysfunction is a typical feature

for example amyotrophic lateral sclerosis (Girardi et al., 2011; Woolley et al., 2011) and

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Parkinson’s disease (Pedersen et al., 2009). However, questionnaires typically include

statements that rely on performing physical activity and apathy measurement may be falsely

inflated as a consequence (Goldstein and Abrahams, 2013).

The aim of this research was to develop a new method of assessing apathy, the

Dimensional Apathy Scale (DAS), a multi-dimensional approach based on Levy and Dubois’

(2006) apathetic subtypes. Furthermore, in order to accommodate for the assessment of

apathy in patients with motor dysfunction the scale was designed to minimize exaggeration of

symptom due to physical disability.

Specifically, published scales were initially reviewed to identify questions, which

would yield a triadic structured questionnaire according to Levy and Dubois’ (2006)

apathetic subtypes and produce the DAS. Firstly, the psychometric properties of this 45-item

scale were initially investigated and a 24-item scale developed. Secondly, the relationship

between performance on the new scale and a standardized measure of depression was

explored.

2. Method

2.2. Participants

A total of 311 participants (217 females and 94 males) were recruited from the

University of Edinburgh Departmental volunteer panel, the University of Hull and other

volunteer groups. The majority of participants came from the University of Edinburgh

Departmental volunteer panel. Participants were only asked to take part if they were healthy

and the volunteer panel database was pre-screened to exclude participants with medical

conditions. Table 2 shows the breakdown of sample characteristics. The study was approved

by the University of Edinburgh, School of Philosophy, Psychology and Language Sciences

(Psychology) Ethics committee.

Table 2. Sample Characteristics Questionnaire

Type

N Mean Age (SD) Min Age Max Age Mean YOE (SD)

Online 266 37.7 (14.7) 20 67 17.3 (3.0)

Paper and pencil 50 35.6 (16.5) 18 70 16.8 (2.7)

Total 311 37.4 (15.0) 18 70 17.2 (3.0)

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2.3. Item Development

A deductive scale development method (Clark and Watson, 1995) was utilized.

Firstly, apathy domains were defined by the characteristics of the Emotional-affective, Auto-

activation and Cognitive Levy and Dubois (2006) apathy subtypes (see Table 1). This was

followed by a review of total of 180 items from 12 existing English apathy scales and

subscales (shown in Table 3). Additionally, items that evaluated executive functioning based

on the Behavioural Assessment of Dysexecutive Syndrome-DEX (Norris and Tate, 2000),

Frontal Systems Behaviour scale (Grace et al., 1999) and the Brief Psychiatric Rating scale

(Overall and Gorham, 1962), were included in the review because they were found to be

consistent with the definition of Cognitive apathy subtype.

Following the review, common themes which were concordant with definitions of the

three dimensions of apathy were determined by the two authors from the 180 existing items,

which was followed by a structured design of new items, resulting in a new 45-item scale1.

Both positive and negative syntax were employed when writing the new items. The new

items were designed to be self- rated using the 4-point Likert scale (Hardly Ever,

Occasionally, Often, Almost always) on rate of occurrence in the last month. Scoring was 0,

1, 2, 3 respectively, with reverse scoring for some items.

                                                                                                               1  See  Supplementary  material  

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Table 3. Apathy scales reviewed in development of DAS Scale Type Number of

Items

Extracted

Reference

Apathy Inventory Full 8 Robert et al. (2002)

The Behavioural Assessment of

Dysexecutive Syndrome- DEX

Sub-scale 20 Norris and Tate (2000)

Brief Psychiatric Rating scale Sub-scale 5 Overall and Gorham

(1962)

Dementia Apathy Interview and

Rating

Full 16 Strauss and Sperry (2002)

Apathy Evaluation Scale Full 18 Marin et al. (1991)

Frontal Systems Behaviour scale Sub-scale 27 Grace et al. (1999)

Irritability Apathy scale Sub-scale 5 Burns et al. (1990)

Key Behaviour Change Inventory Sub-scale 28 Belanger et al. (2002)

Lille Apathy Rating scale Full 28 Sockeel et al. (2006)

Neuropsychiatric Inventory Sub-scale 9 Cummings et al. (1994)

Positive and Negative Symptoms

scale

Sub-scale 8 Kay et al. (1989)

Assessment of Negative Symptoms Sub-scale 8 Andreasen (1982)

2.4. Procedure

Two hundred and sixty six participants completed an online 45-item questionnaire

using Limesurvey, a free and open source survey software tool. Fifty participants completed a

paper and pencil version of the 45-item questionnaire accompanied by completion of the

Becks Depression inventory II (BDI-II; Beck et al., 1996) either at the University of

Edinburgh or in the participant’s home. All participants were informed that if they had any

existent medical or psychiatric conditions, they were not eligible to participate in this study.

As there were no significant differences between the participant characteristics or responses

of those who completed the online and paper and pencil versions the dataset was combined to

investigate the psychometric properties of the items.

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2.5. Statistical analysis

In stage 1 of the analysis a Monte-Carlo based simulation, Horn’s parallel analysis of

principal factors (Horn, 1965, Turner, 1998), was used in comparing eigen values derived

from uncorrelated normal variables to the observed eigen values. It was used to determine the

number of factors to be extracted. An exploratory factor analysis was conducted on the 311

responses to the 45 items with a factor loading cut off of ≥ 0.350 (Kline, 1994) to determine

the factorial substructure of the scale.

In stage 2, inter-item and item-subscale total correlational analysis (Pearson product

moment correlation) was performed for the 24 items of the new scale. Subscale total was

calculated by summing values of items associated with each subscale.

In stage 3, data from the 50 participant subsample who performed the paper and

pencil version of the 45 item scale was used to explore relationship between depression and

subscale item total scores of the 24 items of the new scale. This was done using Pearson

product moment correlation.

3. Results

3.1. Stage 1- Factorial Substructure

Due to the larger number of female participants in the sample; a regression analysis

was initially undertaken on each item response in relation to gender from which the residuals

were extracted. Through examination of histograms and kurtosis of item responses, they were

shown to be normally distributed. The Kaiser-Meyer-Olkin (KMO) and Mean Measure of

Sample Adequacy (MSA) showed the sample to be factorable (KMO = 0.837, Mean MSA =

0.800). Horn’s parallel analysis of principal factors, the use of the characteristic “elbow” or

steep decline in eigen values (Cattell, 1966), indicated four factors to be extracted.

An Exploratory Principle Axis Factor Analysis with Promax (Oblique) rotation- due

to factor 1 (PA1) and factor 4 (PA4) being inter-correlated was used for data analysis (see

Table 4). Eleven items were excluded due to them not meeting the ≥ 0.350 factor loading cut-

off. The 4-factor solution cumulatively accounted for 28.9% of the total variance. This was

further supported by visual inspection and a suitable square root mean residual (SRMR <

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0.05). The factors were subsequently labelled based on the themes of the items loading on to

them.

Table 4. Oblique rotation Exploratory Principle Axial Factor analysis and factor labels Executive (Ex), Emotional (Em), Cognitive Initiation (CI) and Behavioural Initiation (BI) Numbered

Factor

Factor Labels Eigen Values Proportion %

Variance

Cumulative %

Variance

Number of

items

PA1 Ex 5.785 12.9 12.9 17

PA4 Em 2.784 6.2 19.0 8

PA3 CI 2.373 5.3 24.3 5

PA2 BI 2.067 4.6 28.9 5

Seventeen items loaded on PA1, accounting for 12.9% of the total variance, one of

which loaded negatively. It is clear that items loading on PA1 were similar to that described

by Levy and Dubois as the Cognitive apathy subtype. However, the items specifically related

to processes of organisation, (e.g. “When doing a demanding task, I have difficulty working

out what to do”), attention (e.g. “I find it difficult to keep my mind on things”) and planning

(e.g. “I set goals for myself”) abilities. As such these processes may be best described under

the umbrella of executive functions (Burgess and Alderman, 2004). This factor was

subsequently labelled as Executive apathy. A total of eight items were subsequently used to

create the Executive apathy subscale according to their high loadings. Some higher loading

items were not used due to their respective similarities to other items.

Eight items loaded on PA4, accounting for 6.2% of the total variance. There was an

emotional theme to this item cluster similar to the Emotional-affective subtype defined by

Levy and Dubois. However, the items contained no reference to integration aspects of the

Emotional-affective subtype but only that of processing, (e.g. “Before I do something I think

about how other would feel about it”) recognition (e.g. “I struggle to empathise with other

people”) and expression (e.g. “I become emotional easily when watching something happy or

sad on TV”). This factor was subsequently labelled as Emotional apathy. All eight items were

retained for the Emotional apathy subscale part of the 24-item scale.

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Five items loaded on factor 3 (PA3) and five items loaded on factor 2 (PA2),

accounting for 5.3% and 4.6% of the total variance, respectively. Thematically, both factors

were associated with initiation corresponding to the Auto-activation apathy subtype. Items

loading on PA2 (e.g. “I plan my days activities in advance”) were labelled as Behavioural

Initiation apathy while items loading on PA3 (e.g. “I am spontaneous”) were

characteristically more oriented to Cognitive Initiation apathy independent of direct physical

activity. Due to the overlapping thematic similarities between PA2 and PA3 alongside being

the only factors that contained an item that showed overlapping, above threshold loading (“I

think of new things to do during the day”), the items loading on these factors were combined

to make a Behavioural or Cognitive Initiation subscale. One item was not used as a

Behavioural/Cognitive Initiation subscale measure due to its low loading on PA2 with eight

subscale items being retained. This resulted in eight items per apathy subscale that were used

to construct the new 24-item apathy scale, the DAS1.

3.2. Stage 2- Inter-item and Item-Subscale Total Correlations

The following analysis was undertaken on the 24 DAS items only. Internal

consistency reliability was established using Cronbach’s standardized α. Between items α

value for the 24-item scale was 0.798. The item-subscale total correlations were found to be

moderate for each subscale, with the Executive subscale correlating most highly (mean r =

0.639, SD = 0.081), followed by the Behaviour/Cognitive Initiation subscale (mean r =

0.541, SD = 0.085) and then the Emotional subscale (mean r = 0.495, SD = 0.133). However,

item A16 (“I express/ show my emotions”) assessing the Emotional subscale was found to be

of a low correlation (r = 0.191), which resulted in adjustment of the wording to “I express my

emotions” for inclusion in the DAS.

The relationship between subscales total was explored through correlational analysis.

The Executive subscale total was found to be most strongly correlated with the

Behaviour/Cognitive Initiation subscale total (r = 0.648, p<0.001) while being least

correlated with the Emotional subscale total (r = 0.091, NS), indicating a stronger apathetic

executive association with lack of initiation rather than emotional processing. The

Behaviour/Cognitive Initiation subscale total held a weak correlation with the Emotional

subscale total (r = 0.236, p<0.001).

                                                                                                               1  See  Supplementary  material  

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3.3. Stage 3- Depression and Subscale Item Total Correlations

The mean BDI-II score from the fifty participants was 5.6 (SD = 5.4), with a

range of 0 to 24, which contained no severely depressed participants. All subscale total scores

form the 50 participant subsample held moderate positive correlations with depression. BDI-

II was most positively and highly correlated with the Executive subscale total (r = 0.553,

p<0.001) while the Behaviour/Cognitive Initiation total (r = 0.354, p<0.05) and Emotional

total (r = 0.365, p<0.01) subscales were less positively correlated.

4. Discussion

The devised scale was composed of a 4 factor structure akin to Levy and Dubois’

(2006) apathetic subtypes and allowing for the creation of a new three dimensional

assessment of apathy, the DAS, with Emotional, Executive and Cognitive/Behavioural

Initiation subscales.

The Executive factor/subscale was most comparable to Levy and Dubois’ Cognitive

apathy subtype in that it pertained to organization of thoughts and actions. However it

specifically was associated with problems of organization, attention and planning, which as

such fall under the umbrella of executive functions (Burgess and Alderman, 2004). Research

has shown an association between executive dysfunction and apathy in neurodegenerative

disease populations (e.g. Esposito et al., 2010; Varaneseet al., 2011). The items derived for

the Emotional subscale did not meet the Emotional-affective subtype definition. Levy and

Dubois’ definition refers to expression, processing and recognition whereas the Emotional

subscale items referred to integration of emotional behaviours. Therefore, renaming this

subtype to Emotional was justified as it is seems to encompass more collective aspects of

emotional apathy. The Cognitive and Behavioural Initiation factors and subsequent combined

subscale was most similar to the Auto-activation apathy subtype due to the focus being on

both initiation of thought and behaviours. However, the Auto-activation apathy subtype was

primarily defined by lack of motor responsiveness whereas the themes of the behaviour and

cognitive initiation factors were more independent of motor functions. This type of initiation

apathy relates to research in to the ‘Energization’ aspect of executive functioning (Stuss,

2011), which is defined by initiation and sustained response to tasks such as verbal fluency.

Increased apathy levels have been observed as a significant predictor of verbal fluency

deficits in amyotrophic lateral sclerosis patients (Grossman et al., 2007). Upon closer

examination of the two factors, an apparent thematic overlap was found. An example of this

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is was the Cognitive Initiation and Behaviour Initiation factors produced the only overlapping

above threshold item (“I think of new things to do during the day”). The phrasing of this

particular item suggests that there is a relationship between cognition (“think of”) and

behaviour (“to do”) primarily based on initiation (“new things”). Due to this overlap and the

generally mutual features between items loading on to these two factors, they were combined

to produce the Behaviour/Cognitive Initiation subscale.

The new 24-item DAS contained a mixture of negatively and positively phrased items

in an attempt to control for acquiescence and social desirability bias. The eight items chosen

to assess each subtype were detailed in evaluating symptomatic or syndromatic

characteristics related to apathy independent of physical disability. An example of this would

be the wording of some items as to avoid direct reference to motor actions. The questionnaire

will therefore be suitable to assess apathy in patients with neurodegenerative disease and

motor dysfunction such as Parkinson’s disease (Pedersen et al., 2009) and Motor Neurone

Disease (Goldstein and Abrahams, 2013).

The methodical, theory-based item design and thorough examination of established

items from apathy scales and subscales (for review see Clarke et al., 2011) aimed to increase

the effectiveness of this measure. The use of standardized scoring in the form of a Likert

scale as a part of the DAS allowed for more efficient measurement of apathy subtypes.

Limiting each item to only four choices of response attempted to eliminate possible central

tendency bias. Additionally, the internal consistency reliability was high. The item-subscale

total correlations were found to be satisfactory.

The apathy scores for each subscale were all found to be positively, moderately

associated with depression, but at varying degrees. This is most likely due to the overlap

between symptoms of apathy and depression (Levy et al., 1998, van Reekum et al., 2005). In

dementia, psychomotor slowing, and deficits in interest, energy and insight have been found

to be common in depression and apathy (for review see Ishizaki and Mimura, 2011). A

previous review by Tagariello et al. (2009) found at a neurobiological level both apathy and

depression relate to decreased activity of frontal, parietal and temporal regions but found

apathy to be more related to hypoperfusion of fronto-subcortical regions. At a

neurotransmitter level, medications that relieve depression often increase apathy and

medication that decreases apathy are not effective antidepressants (Tagariello et al., 2009).

13    

This discrepancy between behavioural symptoms and neural correlates of the two suggests a

dissociation between depression and apathy that should further be explored. The low and

moderate correlations of the Behaviour/Cognitive Initiation and Emotional subscale total

scores with depression could also be interpreted as a degree of separation of these subscales

from depression or its influence. The Executive subscale was most highly, albeit moderately,

associated with depression. Depression affects a variety of cognitive functions and there is a

well-established relationship of impaired executive functioning in depressed individuals (for

review see McClintock et al., 2010).

This study investigated apathy in a healthy, normal sample and future studies will

look at the structure of apathy and the neuropsychological impairments that are associated

with it. However, this relative or selective apathy is observable in a normative population

(Marin, 1990; Brodaty et al., 2010); therefore measurable to a diminished severity and

variability. We were unable to include the Brief Negative Symptoms Scale (Kirkpatrick et al.,

2011) and the Clinical Assessment Interview for Negative Symptoms (Kring et al., 2013) in

our item development because they were published after the production of the items for the

DAS. These two scales are novel and still underused in research and clinical practice so

might not have been suitable at this stage of development.

In Alzheimer’s disease patients apathy prevalence in patients was found to be 61% to

92% (e.g. Landes et al., 2005) with an almost equally high prevalence in frontotemporal

dementia patients (Mendez et al., 2008). Over a third of Parkinson’s disease patients have

been found to exhibit apathy (e.g. Pedersen et al., 2009; Pluck and Brown, 2002) with

marked variability of its effects on the clinical presentation of Parkinson’s disease (Dujardin

et al., 2007). Neuroimaging of patients with amyotrophic lateral sclerosis has shown evidence

of neuroanatomical correlates relating to apathy and abnormalities in the anterior cingulate

gyrus (Woolley et al., 2011). Due to this high prevalence of apathy in a variety of

neurodegenerative diseases, the will be an effective method of exploring specific dysfunction

of apathetic subtypes within neurological populations.

In conclusion, we have designed a scale, which shows an inherent sub-dimensional

structure of apathy in a healthy population. This multi-dimensional scale for detecting apathy

subtypes has been designed with intended use in neurodegenerative populations specifically

with motor disability. Future research will validate the relationship between these subscales

14    

and determine whether specific subtypes of apathy are disproportionately affected in

neurodegenerative diseases. Identification of pathological apathy subtypes will have further

implications on choosing the appropriate intervention and care pathway for the individual.

References

Blanchard, J. J., Cohen, A. S., 2006. The structure of negative symptoms within

schizophrenia: implications for assessment. Schizophrenia Bulletin, 32(2), 238-245.

Beck, A. T., Steer, R. A., Brown, G. K., 1996. Manual for the Beck Depression Inventory,

Second Edition (BDIII). San Antonio, TX: The Psychological Association.

Belanger, H. G., Brown, L, M., Crowell, T. A., Vanderploeg, R. D., Curtiss, G., 2002. The

Key Behaviors Change Inventory and executive functioning in an elderly clinic

sample. The Clinical Neuropsychologist, 16, 251–257.

Brodaty, H., Altendorf, A., Withall, A., Sachdev, P., 2010. Do people become more apathetic

as they grow older? A longitudinal study in healthy individuals. International

Psychogeriatrics, 22, 426–436.

Burgess, P. W. Alderman, N. 2004. Executive dysfunction. In: L. H. Goldstein L. H.,

McNeil, J. E. (Eds.), Clinical neuropsychology: A practical guide to assessment and

management for clinicians. Chichester, UK: Wiley, pp. 185-209.

Burns, A., Folstein, S., Brandt, J., Folstein, M., 1990. Clinical assessment of irritability,

aggression, and apathy in Huntington and Alzheimer disease. Journal of Nervous and

Mental Disease, 178, 20–26.

Cattell, R. B., 1966. The scree test for the number of factors. Multivariate Behavioral

Research, 1, 245–276.

Chase, T. N., 2011. Apathy in neuropsychiatric disease: diagnosis, pathophysiology and

treatment. Neurotoxicity Research, 19, 266–278.

15    

Clark, L. A., Watson, D. 1995. Constructing validity: Basic issues in objective scale

development. Psychological assessment, 7(3), 309-319.

Clarke, D. E., Ko, J. Y., Kuhl, E. A., van Reekum, R., Salvador, R., Marin, R. S., 2011. Are

the available apathy measures reliable and valid? A review of the psychometric

evidence. Journal of Psychosomatic Research, 70, 73–97.

Cummings, J. L., Mega, M., Gray, K., Rosenberg-Thompson, S., Carusi, D. A., Gornbein, J.,

1994. The Neuropsychiatric Inventory: comprehensive assessment of

psychopathology in dementia. Neurology, 44, 2308–2314.

Dujardin, K., Sockeel, P., Devos, D., Delliaux, M., Krystkowiak, P., Destee, A., Defebvre,

L., 2007. Characteristics of apathy in Parkinson’s disease. Movement Disorders, 22,

778–784.

Esposito, F., Rochat, L., Van der Linden, A. C. J., Lekeu, F., Quittre, A., Charnallet, A., Van

der Linden, M. 2010. Apathy and executive dysfunction in Alzheimer

disease. Alzheimer Disease & Associated Disorders, 24(2), 131-137.

Foussias, G., Remington, G. 2010. Negative symptoms in schizophrenia: avolition and Occam's razor. Schizophrenia Bulletin, 36(2), 359–369.

Fuster, J. M., 1999. Synopsis of function and dysfunction of the frontal lobe. Acta

Neurologica Scandinavia, 99, 51–57.

Girardi, A., MacPherson, S. E., Abrahams, S. 2011. Deficits in emotional and social

cognition in amyotrophic lateral sclerosis. Neuropsychology, 25(1), 53.

Goldstein, L. H., Abrahams, S., 2013. Changes in cognition and behaviour in amyotrophic

lateral sclerosis: nature of impairment and implications for assessment. The Lancet

Neurology, 12(4), 368–380.

Grace, J., Malloy, P., 2001. Frontal Systems Behavior Scale (FrSBe): Professional Manual.

Lutz, FL, Psychological Assessment Resources.

16    

Grace, J., Stout, J. C., Malloy, P. F., 1999. Assessing frontal lobe behavioural syndromes

with the Frontal Lobe Personality Scale. Assessment, 6, 269–284.

Grossman, A. B., Woolley-Levine, S., Bradley, W. G., Miller, R. G. 2007. Detecting

neurobehavioral changes in amyotrophic lateral sclerosis. Amyotrophic Lateral

Sclerosis, 8(1), 56-61.

Habib, M., 2004. Athymhormia and disorders of motivation in basal ganglia disease. Journal

of Neuropsychiatry and Clinical Neuroscience, 16, 509–525.

Horn, J. L., 1965. A rationale and test for the number of factors in factor analysis.

Psychometrika, 30, 179–185.

Ishizaki, J., Mimura, M., 2011. Dysthymia and apathy: diagnosis and treatment. Depression

research and treatment, 1–7, doi:10.1155/2011/893905.

Kay, S. R., Opler, L. A., Lindenmayer, J. P., 1989. The Positive and Negative Syndrome

Scale (PANSS): rationale and standardisation. British Journal of Psychiatry, 155, 59–

67.

Kirkpatrick, B., Strauss, G. P., Nguyen, L., Fischer, B. A., Daniel, D. G., Cienfuegos, A.,

Marder, S. R., 2011. The brief negative symptom scale: psychometric

properties. Schizophrenia bulletin, 37(2), 300-305.

Kline, P., 1994. An easy guide to factor analysis. London: Routledge.

Kring, A. M., Gur, R. E., Blanchard, J. J., Horan, W. P., Reise, S. P., 2013. The clinical

assessment interview for negative symptoms (cains): final development and

validation. American Journal of Psychiatry, 170(2), 165-172

Landes, A. M., Sperry, S. D., Strauss, M. E., 2005. Prevalence of apathy, dysphoria, and

depression in relation to dementia severity in Alzheimer's disease. The Journal of

Neuropsychiatry and Clinical Neuroscience, 17, 342–349.

17    

Levy, R., 2012. Apathy: A pathology of goal-directed behaviour. A new concept of the clinic

and pathophysiology of apathy. Revue neurologique, 168(8), 585–597.

Levy, M. L., Cummings, J. L., Fairbanks, L. A., Masterman, D., Miller, B. L., Craig, A. H.,

Paulsen, J. S., Litvan, I., 1998. Apathy is not depression. The Journal of

Neuropsychiatry and Clinical Neuroscience, 10, 314–319.

Levy, R., Czernecki V., 2007. Apathy and the basal ganglia. Journal of Neurology, 253, 54–

61.

Levy, R., Dubois, B. 2006. Apathy and the functional anatomy of the prefrontal cortex-basal

ganglia circuits. Cerebral Cortex, 16, 916–928.

Marin, R. S., 1990. Differential diagnosis and classification of apathy. The American Journal

of Psychiatry, 147(1), 22-30.

Marin, R. S., 1991. Apathy: a neuropsychiatric syndrome. Journal of Neuropsychiatry and

Clinical Neuroscience, 3, 243–254.

Marin, R. S., 1996. Apathy: concept, syndrome, neural mechanisms, and treatment. Seminars

in Clinical Neuropsychiatry, 1, 304–314.

Marin, R. S., Biedrzycki, R. C., Firinciogullari, S., 1991. Reliability and validity of the

Apathy Evaluation Scale. Psychiatry Research, 38, 143–162.

Marin, R. S., Firinciogullari, S., Biedrzycki, R. C., 1994. Group differences in the

relationship between apathy and depression. Journal of Nervous and Mental Disease,

182, 235–239.

Mendez, M. F., Lauterbach, E. C., Sampson, S. M., 2008. ANPA Committee on Research.

An evidence-based review of the psychopathology of frontotemporal dementia: a

report of the ANPA Committee on Research. The Journal of Neuropsychiatry and

Clinical Neuroscience, 20, 130–149.

18    

McClintock, S. M., Husain, M. M., Greer, T. L., Cullum, C. M., 2010. Association between

depression severity and neurocognitive function in major depressive disorder: A

review and synthesis. Neuropsychology, 24, 9–34.

Norris, G., Tate, R. L., 2000. The behavioural assessment of the dysexecutive syndrome

(BADS): ecological, concurrent and construct validity. Neuropsychological

Rehabilitation, 10, 33–45.

Overall, J. E., Gorham, D. R., 1962. The Brief Psychiatric Rating Scale. Psychological

Reports, 10, 790–812.

Pluck, G. C., Brown, R. G., 2002. Apathy in Parkinson’s disease. Journal of Neurology,

Neurosurgery and Psychiatry, 73, 636–642.

Pedersen, K. F., Larsen, J. P., Alves, G., Aarsland, D., 2009. Prevalence and clinical

correlates of apathy in Parkinson’s disease: a community-based study. Parkinsonism

& Related Disorders, 15, 295–299.

Robert, P. H., Clairet, S., Benoit, M., Koutaich, J., Bertogliati, C., Tible, O., Caci, H., Borg,

M., Brocker, P., Bedoucha, P., 2002. The Apathy Inventory: assessment of apathy and

awareness in Alzheimer's disease, Parkinson's disease and mild cognitive impairment.

International Journal of Geriatric Psychiatry, 17, 1099–1105.

Robert, P. H., Onyike, C. U., Leentjens, A. G. F., Dujardin K., Aalten, P., Starkstein, S.,

Verhey, F. R. J., Yessavage, J., Clement, J. P., Drapier, D., Bayle, F., Benoit, M.,

Boyer, P., Lorca, P. M., Thibaut, F., Gauthier, S., Grossberg, G., Vellas, B., Byrne, J.,

2009. Proposed diagnostic criteria for apathy in Alzheimer’s disease and other

neuropsychiatric disorders. European Psychiatry, 24, 98–104.

Sockeel, P., Dujardin, K., Devos, D., Deneve, C., Destee, A., Defebvre, L., 2006. The Lille

Apathy Rating Scale (LARS), a new instrument for detecting and quantifying apathy:

19    

validation in Parkinson's disease. Journal of Neurology, Neurosurgery and Psychiatry,

77, 579–584.

Starkstein, S. E., Leentjens, A. F. 2008. The nosological position of apathy in clinical

practice. Journal of Neurology, Neurosurgery & Psychiatry, 79(10), 1088-1092.

Strauss, M. E., Sperry, S. D., 2002. An informant-based assessment of apathy in Alzheimer

disease. Neuropsychiatry, Neuropsychology, & Behavioral Neurology, 15, 176–183.

Stuss D. T., 2011. Functions of the frontal lobes: relation to executive functions. Journal of

the International Neuropsychological Society, 17, 759–765.

Tagariello, P., Girardi, P., Amore, M., 2009. Depression and apathy in dementia: same

syndrome or different constructs? A critical review. Archives of gerontology and

geriatrics, 49(2), 246–249.

Turner, N. E., 1998. The effect of common variance and structure pattern on random data

eigenvalues: Implications for the accuracy of parallel analysis. Educational and

Psychological Measurement, 58, 541–568.

Woolley, S. C., Zhang, Y., Schuff, N., Weiner, M. W., Katz, J. S., 2011. Neuroanatomical

correlates of apathy in ALS using 4 Tesla diffusion tensor MRI. Amyotrophic Lateral

Sclerosis, 12, 52–58.

van Reekum, R., Stuss, D. T., Ostrander, L., 2005. Apathy: why care? The Journal of

Neuropsychiatry and Clinical Neuroscience, 17, 7–19.

Varanese, S., Perfetti, B., Ghilardi, M. F., Di Rocco, A. 2011. Apathy, but not depression,

reflects inefficient cognitive strategies in Parkinson's disease. PLoS One, 6(3),

e17846.

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Developing a new apathy measurement scale: dimensional apathy scale

Ratko Radakovic and Sharon Abrahams

This material supplements but does not replace the content of the peer-reviewed paper published in Psychiatry Research.

45-item scale Item  Code   Item  A1   I find it hard to concentrate on things A2   I am affectionate to those I care about A3   I have difficulty thinking of things to do A4   I need a bit of encouragement to get things started A5   I am not interested in other people's news A6   I feel emotionally flat A7   I contact my friends A8   I become emotional easily when watching something happy or sad on TV A9   I am unconcerned about how others feel about my behaviour A10   I lack motivation A11   After having done something, I spend time thinking whether it was good or bad A12   I find myself staring in to space A13   Before I do something I think about how others would feel about it A14   I plan my days activities in advance A15   I struggle to empathise with other people A16   I express/ show my emotions A17   I try new things A18   I am easily distracted A19   When faced with several options, I arrive to a decision easily A20   When criticized I feel the need to defend myself A21   I am a good problem solver A22   I sit and think of nothing for most of the day A23   I set goals for myself A24   I act on things I have thought about during the day A25   I am organized A26   I need to be prompted to perform everyday tasks A27   When doing a demanding task, I have difficulty working out what I have to do A28   I keep myself busy A29   I get easily confused when doing several things at once A30   My mind tends to go blank A31   I struggle to keep track of conversation A32   I think of new things to do during the day A33   I find it difficult to keep my mind on things A34   I am concerned about how my family feel A35   I am able to focus on a task until it is finished A36   I feel indifferent to what is going on around me A37   When I want to do something I can make an effort A38   I am uninterested in what others have to say A39   If I think I will forget something, I make an effort to remember it A40   I am spontaneous A41   When I make a mistake, I try and correct A42   When I can, I start conversations A43   I am not concerned about failing or succeeding A44   When I receive bad news I feel bad about it

21    

A45   I sometimes start things but find it hard to finish them

22    

Note. Positive scored items *

23    

SELF- DAS (DIMENSIONAL APATHY SCALE) Scoring Instructions Using the scoring instructions below, sum the total scores for each subscale. Scoring Instructions Positive Item Scoring + Negative Item Scoring

◊ Almost always ◊ Often ◊ Occasionally ◊ Hardly Ever

0 1 2 3

◊ Almost always ◊ Often ◊ Occasionally ◊ Hardly Ever

3 2 1 0

Scoring Sheet Executive Subscale Item Score 1 6 10+ 11 17 19 21 23

Total:

Emotional Subscale

Item Score 3+ 5+ 7+ 9+ 12 15 20+ 24

Total:

Behaviour/Cognitive Initiation Subscale

Item Score 2+ 4+ 8+ 13+ 14+ 16+ 18+ 22+

Total: